Abstract
Potentially toxic elements (PTEs) pollution has become a serious environmental threat, particularly in develo** countries such as China. In response, there is a growing interest in phytoremediation studies to identify plant species as designated hyperaccumulators of PTEs in polluted soils. Poinsettia was selected as a candidate species for phytoremediation of six PTEs (Zn, Pb, Hg, Cr, As, Cu) in this study. A pot cultivation experiment (randomized incomplete block experimental design with 5 treatments and 4 blocks) was conducted using contaminated soils gathered from an industrial area in southcentral China. The bioaccumulation factor (BAF), translocation factor (TF), and bioconcentration factor were analyzed to determine the phytoremediation potential of poinsettia potted in different ratios of polluted soils. One-way ANOVA with post-hoc Tukey’s test showed that poinsettia had significant uptake of Zn, Pb, Cu (BAF < 1 and TF < 1, p < 0.05) and Hg (BAF < 1 and TF > 1, p < 0.05). Poinsettias can therefore effectively accumulate Zn, Pb, and Cu in their lateral roots while extracting and transferring Hg into their leaves. Moreover, poinsettia exhibited tolerance towards As and Cr. Interestingly, it was also observed that PTEs can inhibit the height of potted poinsettia at a certain concentration.
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Introduction
The term "potentially toxic elements" (PTEs), more commonly known as "heavy metals", is considered more appropriate than "toxic" or "heavy metal" as a grou** name for metal(loid)s related to pollution and potential toxicity (Duffus 2002; Shaheen et al. 2013; Pourret and Bollinger 2018). The main reason is that heavy metal, defined as elements with a density greater than 7 g cm−3 (other authors choose different limits), does not have biological significance, chemical basis, and definition of authority (Smith 1996; Duffus 2002; Hodson 2004; Madrid 2010; Chapman 2012). In contrast, "Trace elements" (TEs) are associated with their abundance and include metals, metalloids, non-metals, and other elements in soil–plant-animal systems (Shaheen et al. 2013). High concentrations of some TEs like Zn, Pb, Cu, Cr, As, Cd, and Ni are potentially toxic to organisms and may pose long-term risks to ecosystems by circulating in the food web (Arif et al. 2016; Antoniadis et al. 2019).
PTEs pollution has become a pervasive problem globally that poses severe threats to humans and the environment (Cojocaru et al. 2016; Sarwar et al. 2017). The main anthropogenic causes of PTEs pollution are discharged waste from industry and mining, the overuse of agricultural chemicals, sewage sludge used in irrigation, and improper treatment of waste (Odukoya et al. 2018; Yang et al. 2018). In China, the concentrations of PTEs in soils and sediments around factories were estimated to be as high as 36.3%, which is well above the national standard (China 2018). Excessive quantities of PTEs through runoff decrease the quality and productivity of soils and lead to their accumulation in crops, potentially endangering human health (Yang et al. 2018; Khan et al. 2019). For example, excessive Zn intake can lead to depression, prostate cancer, and other chronic diseases (Li et al. 2019). Pb is an extremely toxic metal which have been reported as adversely affecting humans' nervous, endocrine, immune, and circulatory systems (Zhang et al. 2012; Chen et al. 2016). Moreover, As and Cr have been increasingly found in food crops, which poses a severe carcinogenic risk for China's people (Clemens and Ma 2016; Wang et al. 2018). Given the health and environmental risks of toxic metal(loid)s pollution, it is crucial to identify effective strategies for remediating PTEs- contaminated soils.
Phytoremediation of PTEs contaminated soils is an environmentally-sound technique that is more efficient and cost-effective than traditional physical and chemical techniques (John et al. 2009; Bissonnette et al. 2010; Dixit et al. 2015; Sarwar et al. 2017). Phytostabilization and phytoextraction are two commercially promising sub-phytotechnologies of phytoremediation (Raskin 1995; Salt et al. 1995). Phytostabilization uses plants with dense root systems and vegetation cover to stabilize PTEs in the root zone (Salt et al. 1995; Singh 2012; Antoniadis et al. 2017). Phytoextraction, the most common phytotechnology employed, uses plants to absorb various PTEs from the soil and translocate them to their aerial organs (Raskin 1995; Peng et al. 2009; Antoniadis et al. 2017). Some plants that can tolerate and translocate high PTEs in their aerial organs without toxic symptoms are termed hyperaccumulators (Brooks 1977; Baker and Brooks 1989; Memon and Schroder 2009). Conversely, non-hyperaccumulators (or simply 'accumulators') store PTEs in their roots rather than translocating them to aboveground parts. Investigating the phytoremediation potential of ornamental plants that can be sold commercially can incentivize their use in remediating soils given the added profitability (Schwitzguébel 2015).
Some studies have found various native plants with hyperaccumulation tendencies of PTEs occurring naturally around metallurgy and mining factories (Čudić et al. 2016; Sasmaz et al. 2016). However, these plants are mostly herbaceous annuals with little commercial value, or that cannot be self-sustaining (Moreno-Jiménez et al. 2011). Moreover, since large-scale planting requires substantial initial investments, interest has shifted towards identifying ornamental species with economic benefits or by-product generation to sustain phytoremediation efforts (Chintakovid et al. 2008; Chaturvedi et al. 2014; Nakbanpote et al. 2016). The ornamental plant Euphorbia milli has been shown to effectively remediate moderately-contaminated soils of Cr (Ramana et al. 2015).
Poinsettia (Euphorbia pulcherrima Willd. et Kl.), a perennial shrub of the spurge family (Euphorbiaceae), is a commercially important pot and cut flower species cultivated globally, especially as a Christmas ornamental plant (Mabberley 1997; Allaby 2016). Current breeding research of poinsettia has focused on its cultivation and management techniques (Zhou 2009; Meng 2014). Since poinsettias are commercially more popular than Euphorbia milli, it is of considerable importance to explore whether poinsettia has the remediation potential of PTEs contaminated soils to promote the wide commercial application of phytoremediation technology. Several studies involving phytoremediation pot experiments have reported that, plants were only exposed to one or two types of PTEs at a time, which may reduce plants to show their true phytoremediation potential due to neglecting the effects of a multi-element environment (Antoniadis et al. 2017). Therefore, in this study, we directly collected the contaminated soil in the industrial area for the pot experiment and studied poinsettia's ability to remediate six common PTEs, including toxic metals (Zn, Pb, Hg, Cr, Cu) and metalloids (As).
Since the large-scale establishment of factories (old industrial areas) began in 1953 in Zhuzhou city of Hunan province in southcentral China, PTEs pollutants have been continually discharged for over 20 years without adequate treatment (Dou et al. 2008). As a result, Zhuzhou has become one of the most PTEs polluted cities in China (Dou et al. 2008). It is of considerable interest to remediate these soils to prevent PTEs from entering the food chain and posing health and environmental risk. Thus, the main aim of this study was to: (1) evaluate the growth of poinsettia in industrial soils contaminated by PTEs; (2) evaluate the hyperaccumulation and phytoremediation potential of poinsettia for Zn, Pb, Hg, Cr, As, Cu.
Materials and methods
Study sites and soil collection
Soils were collected from ** lead–zinc mine area. China Environ Int 30:567–576" href="/article/10.1007/s12298-021-00980-w#ref-CR77" id="ref-link-section-d84647832e2785">2004; Yoon et al. 2006; Cui et al. 2007; Li et al. 2007; Malik et al. 2010; Bedabati Chanu and Gupta 2016; Cojocaru et al. 2016). In this study, poinsettia had a BCF > 1 and TF < 1 when Zn, Pb, and Cu were analyzed, indicating the potential for phytostabilization (Yoon et al. 2006). On the contrary, the poinsettia can transport a high level of Hg to the leaves (BAF < 1 and TF > 1), suggesting its potential for phytoextraction (Were et al. 2017). Interestingly, there are more Cr and As taken up in roots and leaves of the control group compared to 100% treatment group. For Cr, it is essential to clarify that only 75% and 100% of the treatment groups had soil Cr levels above the standard before the experiment. Therefore, poinsettias grown in soil with Cr overload may inhibit Cr uptake in the lateral roots, and the Cr in the leaves may have been transferred to the stems (Singh et al. 2013). However, the TF of Cr tends to approach 1 with the increase of PTEs content in the soil, indicating that poinsettia may have the potential of phytoextraction of Cr. Furthermore, the TF value of Cr in the 100% treatment group of poinsettias (TF = 0.76) was higher compared to the Euphorbia mill (TF = 0.73), which was considered to have phytoremediation potential (Ramana et al. ). More particularly, As was more severely exceeded in non-industrial soils compared to that in industrial soils before the experiment. As the soil As cont2015ent increased, the As levels in lateral roots and leaves increased while that in primary roots and stems decreased. Nevertheless, poinsettia had no phytoremediation for As because the indices were all far less than 1. Further, field experiments are needed to observe the phytoremediation of poinsettias on PTEs, as phytoremediation can be assisted in pot experiments by amendments of releasing agents, but the remediation factors may be lower under real field conditions (Neugschwandtner et al. 2008; Chen et al. 2016).
The results indicated that the poinsettia concentrated PTEs mainly in the lateral roots. This was consistent with the fact that many ornamental plants accumulated PTEs in their roots (Chintakovid et al. 2008; Trigueros et al. 2012; Cui et al. 2013; Chaturvedi et al. 2014; Pérez-López et al. 2014). Therefore, they can be used to remediate contaminated soil to some extent through phytostabilization while landsca** and selling for income. After harvest, the metal-enriched biomass usually needs to be incinerated after harvesting to recover residual PTEs and avoid secondary contamination from plant litter (Nakbanpote et al. 2016). The poinsettia accumulated Zn, Pb, and Cu in the roots, so the aerial organs of poinsettia can still be harvested and marketed as cut flowers for their ornamental value. Moreover, the aerial organs of the poinsettia did not accumulate large amounts of TEs, reducing the risk of transfer of PTEs to the food chain (Dominguez et al. 2008). Thereby, poinsettia may be an essential candidate for the use of Zn, Pb, Cu phytostabilization, and Hg phytoextraction in industrial soils contaminated with PTEs.
Various metal ions dissociated from their complex forms on the surface of the roots and were stored in large amounts in the root branch exosome (Arif et al. 2016). Trees with phytoremediation capabilities absorb PTEs through their extensive root systems and transport them to aerial organs (Vincent et al. 2018). However, their woody characteristic is not conducive to PTEs accumulation (Ahmad 2016). Among the 54 tree species, the maximum absorption of Cu, Pb, and Zn were only 371, 27, and 539 µg g−1 (Shang et al. 2019), all lower compared to the value of poinsettia absorption (486, 155, and 1676 µg g−1). Therefore, shrubs may be more efficient at absorbing PTEs compared to trees. As for herbaceous perennials, they need large planting areas and the mature grasses need to be removed each year promptly. Many herbs can accumulate large amounts of PTEs primarily because of their high biomass (Hou et al., 2020). For example, Pennisetum sp. has higher biomass compared to both the Cd hyperaccumulator Sedum Plumizincicola and the Cu tolerant Elsholtzia splendens, so it can accumulate and remove more Cd and Cu (Xu et al. 2019). From these perspectives, ornamental shrubs may be a better substitute for herbs.
Conclusion
By comparing the growth status of poinsettia in 5 different levels of polluted soils, we deduced the following conclusions. (1) Poinsettia grows well in PTEs contaminated soils, and PTEs (possibly chromium) may be able to control poinsettia plant height. (2) Our study showed poinsettia was not a hyperaccumulator of Zn, Pb, Hg, Cr, As, and Cu. However, poinsettia had the potential of hyperaccumulator for Zn and phytoremediation for Cr, which need to be further studied. (3) Poinsettia characterized high potential for phytoextraction of Hg and phytostabilization of Zn, Pb, and Cu in industrial soils. Besides, it can tolerate As and Cr. In future experiments, methods to improve the TF of Zn, Pb, Hg, and Cu in poinsettia can be studied, such as adding chelators and cooperating with microorganisms to speed up the phytoremediation process. (4) Perennial ornamental shrubs, such as poinsettias, may be more suitable for phytoremediation applications than some trees and herbs.
Availability of data and materials
All data and materials support the published claims and comply with field standards.
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Software application or custom code support the published claims and comply with field standards.
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Acknowledgements
We acknowledge Central South University of Forestry and Technology for providing laboratory and equipment support for our research.
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This study was funded by National Natural Science Foundation of China, grant number 31601780.
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Conceptualization, ZG and YJ; methodology, ZG and YJ; software, FX and HC; validation, ZG and FX; formal analysis, RY and QZ; investigation, PH; resources, RY, PH, LY and QZ; data curation, YJ and FX; writing—original draft preparation, FX; writing—review and editing, AS and ZG; visualization, FX; supervision, ZG; project administration, ZG. All authors have read and agreed to the published version of the manuscript.
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**ao, F., Gu, Z., Sarkissian, A. et al. Phytoremediation of potentially toxic elements in a polluted industrial soil using Poinsettia. Physiol Mol Biol Plants 27, 675–686 (2021). https://doi.org/10.1007/s12298-021-00980-w
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DOI: https://doi.org/10.1007/s12298-021-00980-w